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Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles

The Colorado potato beetle (CPB) is an internationally recognized plant quarantine pest that causes serious losses to potato agricultural production. The gut microbiota plays an important role in its growth and development, and the olfactory system plays an important role in insect feeding behavior....

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Autores principales: Li, Hongwei, Yu, Yanxue, Zhang, Jian, Wang, Yuhan, Zhang, Liu, Zhai, Junfeng, Zhang, Yongjiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10338844/
https://www.ncbi.nlm.nih.gov/pubmed/37455752
http://dx.doi.org/10.3389/fmicb.2023.1197700
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author Li, Hongwei
Yu, Yanxue
Zhang, Jian
Wang, Yuhan
Zhang, Liu
Zhai, Junfeng
Zhang, Yongjiang
author_facet Li, Hongwei
Yu, Yanxue
Zhang, Jian
Wang, Yuhan
Zhang, Liu
Zhai, Junfeng
Zhang, Yongjiang
author_sort Li, Hongwei
collection PubMed
description The Colorado potato beetle (CPB) is an internationally recognized plant quarantine pest that causes serious losses to potato agricultural production. The gut microbiota plays an important role in its growth and development, and the olfactory system plays an important role in insect feeding behavior. The gut microbiota is known to be capable of inducing changes in the olfactory systems of insects. However, the way these associated gut microbes influence the feeding-related behaviors of CPBs remains unclear. To explore the relationship between them, fresh potato leaves immersed in a mixture of five antibiotics (tetracycline, penicillin, ofloxacin, ciprofloxacin, and ampicillin) at specific concentrations for 1 h were fed to adult CPBs to reduce the abundance of gut microbes. We found that the feeding behavior of CPBs was significantly affected by the gut microbiota and that Pseudomonas was significantly higher in abundance in the control group than in the antibiotic group. We then used transcriptome sequencing to explore the differences in olfactory receptor genes in the heads of non-treatment and antibiotic-fed CPBs. Through Illumina Hiseq™ sequencing and screening of differential genes, we found that the olfactory receptor gene LdecOR9 was significantly upregulated and LdecOR17 was significantly downregulated after antibiotic feeding. A real-time polymerase chain reaction was used to verify the changes in olfactory receptor gene expression in the non-treatment groups and antibiotic-treated groups. The feeding behavior was partially rescued after CPBs were re-fed with intestinal bacteria. These results indicate that a certain amount of gut microbiota can result in the loss of the olfactory discrimination ability of CPBs to host plants. In summary, this study investigated the relationship between gut microbiota and olfactory genes, providing a reference for research on microbial control.
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spelling pubmed-103388442023-07-14 Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles Li, Hongwei Yu, Yanxue Zhang, Jian Wang, Yuhan Zhang, Liu Zhai, Junfeng Zhang, Yongjiang Front Microbiol Microbiology The Colorado potato beetle (CPB) is an internationally recognized plant quarantine pest that causes serious losses to potato agricultural production. The gut microbiota plays an important role in its growth and development, and the olfactory system plays an important role in insect feeding behavior. The gut microbiota is known to be capable of inducing changes in the olfactory systems of insects. However, the way these associated gut microbes influence the feeding-related behaviors of CPBs remains unclear. To explore the relationship between them, fresh potato leaves immersed in a mixture of five antibiotics (tetracycline, penicillin, ofloxacin, ciprofloxacin, and ampicillin) at specific concentrations for 1 h were fed to adult CPBs to reduce the abundance of gut microbes. We found that the feeding behavior of CPBs was significantly affected by the gut microbiota and that Pseudomonas was significantly higher in abundance in the control group than in the antibiotic group. We then used transcriptome sequencing to explore the differences in olfactory receptor genes in the heads of non-treatment and antibiotic-fed CPBs. Through Illumina Hiseq™ sequencing and screening of differential genes, we found that the olfactory receptor gene LdecOR9 was significantly upregulated and LdecOR17 was significantly downregulated after antibiotic feeding. A real-time polymerase chain reaction was used to verify the changes in olfactory receptor gene expression in the non-treatment groups and antibiotic-treated groups. The feeding behavior was partially rescued after CPBs were re-fed with intestinal bacteria. These results indicate that a certain amount of gut microbiota can result in the loss of the olfactory discrimination ability of CPBs to host plants. In summary, this study investigated the relationship between gut microbiota and olfactory genes, providing a reference for research on microbial control. Frontiers Media S.A. 2023-06-28 /pmc/articles/PMC10338844/ /pubmed/37455752 http://dx.doi.org/10.3389/fmicb.2023.1197700 Text en Copyright © 2023 Li, Yu, Zhang, Wang, Zhang, Zhai and Zhang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Li, Hongwei
Yu, Yanxue
Zhang, Jian
Wang, Yuhan
Zhang, Liu
Zhai, Junfeng
Zhang, Yongjiang
Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles
title Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles
title_full Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles
title_fullStr Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles
title_full_unstemmed Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles
title_short Gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in Colorado potato beetles
title_sort gut microbiota influences feeding behavior via changes in olfactory receptor gene expression in colorado potato beetles
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10338844/
https://www.ncbi.nlm.nih.gov/pubmed/37455752
http://dx.doi.org/10.3389/fmicb.2023.1197700
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